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An Apoplastic Defensin of Wheat Elicits the Production of Extracellular Polysaccharides in Snow Mold

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An Apoplastic Defensin of Wheat Elicits the Production of Extracellular Polysaccharides in Snow Mold plants Article An Apoplastic Defensin of Wheat Elicits the Production of Extracellular Polysaccharides in Snow Mold Ayako Isobe 1,2, Chikako Kuwabara 1, Michiya Koike 1, Keita Sutoh 1, Kentaro Sasaki 1,3 and Ryozo Imai 1,3,* 1 Hokkaido Agricultural Research Center, National Agriculture and Food Research Organization (NARO), Toyohira-ku, Sapporo 062-8555, Japan; [email protected] (A.I.); [email protected] (C.K.); [email protected] (M.K.); [email protected] (K.S.); [email protected] (K.S.) 2 Graduate School of Life Science, Hokkaido University, Kita-ku, Sapporo 060-0810, Japan 3 Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), 3-1-3 Kannondai, Tsukuba 305-8604, Japan * Correspondence: [email protected]; Tel.: +81-29-838-8378 Abstract: TAD1 (Triticum aestivum defensin 1) is a plant defensin specifically induced by low temper- ature in winter wheat. In this study, we demonstrated that TAD1 accumulated in the apoplast during cold acclimation and displayed antifungal activity against the pink snow mold fungi Microdochium nivale. When M. nivale was treated with TAD1, Congo red-stainable extracellular polysaccharides (EPS) were produced. The EPS were degradable by cellulase treatment, suggesting the involvement of β-1,4 glucans. Interestingly, when the fungus was treated with FITC-labeled TAD1, fluorescent signals were observed within the EPS layer. Taken together, these results support the hypothesis that the EPS plays a role as a physical barrier against antimicrobial proteins secreted by plants. We antici- pate that the findings from our study will have broad impact and will increase our understanding of plant–snow mold interactions under snow. Citation: Isobe, A.; Kuwabara, C.; Keywords: apoplast; cold acclimation; defensin; extracellular polysaccharides; wheat Koike, M.; Sutoh, K.; Sasaki, K.; Imai, R. An Apoplastic Defensin of Wheat Elicits the Production of Extracellular Polysaccharides in Snow Mold. Plants 1. Introduction 2021, 10, 1607. https://doi.org/ Overwintering cereals and perennial grasses in temperate and boreal climate zones 10.3390/plants10081607 must endure prolonged exposure to subzero temperatures. The freezing tolerance of plants substantially increases after a period of exposure to low but non-freezing temperatures, Academic Editor: Aziz Aziz which is a well characterized process known as cold acclimation [1]. In northern areas with deep and persistent snow, winter cereals such as wheat and rye often suffer from Received: 17 July 2021 snow mold diseases caused by fungi such as Microdochium nivale, Typhula ishikariensis, and Accepted: 3 August 2021 Published: 5 August 2021 Sclerotinia borealis, while they are protected from freezing under the snow cover. It has been reported that resistance against snow mold fungus increases during cold acclimation in Publisher’s Note: MDPI stays neutral overwintering plants such as winter wheat [2], barley [3], and Arabidopsis [4]. However, with regard to jurisdictional claims in the mechanism of cold-induced resistance to pathogens is poorly understood. published maps and institutional affil- In order to better understand this process and elucidate the functional mechanisms of iations. this phenomenon, we aimed to clone and functionally characterize novel defense-related genes that are induced during cold acclimation. We identified a plant defensin gene, TAD1 (Triticum aestivum defensin 1), that is specifically induced by cold treatment in winter wheat [5]. Plant defensins are known as a class of the pathogenesis-related (PR) pro- teins [6]. Under in vitro conditions, the recombinant TAD1 protein showed inhibitory Copyright: © 2021 by the authors. Pseudomonas cichorii T. ishikarien- Licensee MDPI, Basel, Switzerland. activity against the plant pathogen and the snow mold This article is an open access article sis [5,7]. Furthermore, overexpression of TAD1 confers resistance against T. ishikariensis in distributed under the terms and wheat [7]. TAD1 is induced by cold and abscisic acid treatment but not by defense-related conditions of the Creative Commons phytohormones such as salicylic acid and methyl jasmonate, suggesting that the gene is Attribution (CC BY) license (https:// under regulation of abiotic signals rather than biotic ones [5]. creativecommons.org/licenses/by/ Here, we report that the TAD1 protein accumulates in apoplasts of wheat leaf tissue 4.0/). during cold acclimation and suggest its involvement in cold-induced resistance against Plants 2021, 10, 1607. https://doi.org/10.3390/plants10081607 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 9 phytohormones such as salicylic acid and methyl jasmonate, suggesting that the gene is Plants 2021, 10, 1607 under regulation of abiotic signals rather than biotic ones [5]. 2 of 8 Here, we report that the TAD1 protein accumulates in apoplasts of wheat leaf tissue during cold acclimation and suggest its involvement in cold-induced resistance against snow molds. We found that M. nivale secretes extracellular polysaccharides in response to TAD1snow treatment, molds. We providing found that functionalM. nivale secretesevidence extracellular for the existence polysaccharides of a defense in mechanism response to ofTAD1 the pathogen treatment, against providing host defense functional systems. evidence for the existence of a defense mechanism of the pathogen against host defense systems. 2. Results 2. Results 2.1.2.1. TAD1 TAD1 Localized Localized in in Extracellular Extracellular Space Space during during Cold Cold Acclimation Acclimation SinceSince TAD1 TAD1 has has putative putative N N-terminal-terminal signal signal peptides peptides [5], [5], it it was was expected expected that that TAD1 TAD1 entersenters into into the the secretary secretary pathway. pathway. We We analyzed analyzed the thesubcellular subcellular localization localization and andaccumu- accu- lationmulation of TAD1 of TAD1 during during cold coldacclimation. acclimation. An immunoblot An immunoblot analysis analysis with polyclo with polyclonalnal anti- bodiesantibodies against against TAD1 TAD1 did not did detect not detect any cross any cross-reacting-reacting bands bands in the in total the totalsoluble soluble fraction frac- (Figuretion (Figure S1). In S1 contrast,). In contrast, a cross a cross-reacting-reacting band band with with a molecular a molecular mass mass of approximately of approximately 6 kDa6 kDa was was detected detected in the in theapoplast apoplast fractions fractions (Figure (Figure 1), which1), which is close is close in size in sizeto that to of that ma- of turemature TAD1 TAD1 protein protein (5.54 (5.54 kDa). kDa). Accumulation Accumulation of the of the TAD1 TAD1 protein protein in in the the apoplast apoplast fraction fraction waswas detectable detectable at at the the first first day day of of cold cold acclimation acclimation and and further further accumulated accumulated during during 14 14 d d of of coldcold acclimation acclimation (Figure (Figure 1B).1B). This This pattern pattern of of accumulat accumulationion was was in in good good accordance accordance with with thatthat of of TAD1TAD1 expressionexpression during during cold cold acclimation acclimation [5]. [5]. FigureFigure 1. 1. WesternWestern blot analysisanalysis ofof cold-acclimated cold-acclimated wheat wheat apoplastic apoplastic protein protein extracts. extracts. (A,B ()A Apoplastic,B) Apo- plasticproteins proteins from a from time a course time course of cold of treatment cold treatment were separated were separated by SDS-PAGE by SDS (A-PAGE), and a(A duplicated), and a du- gel plicatedwas transferred gel was transferred to a membrane to a membrane for Western for blot Western analysis blot (B ).analysis CA, cold (B acclimation.). CA, cold acclimation. 2.2.2.2. Subcellular Subcellular Localization Localization of of TAD1 TAD1-GFP-GFP Protein Protein TheThe subcellular subcellular localization localization of of TAD1 TAD1 was was also also analyzed analyzed using using GFP GFP-fusion-fusion proteins. proteins. TwoTwo ex expressionpression vectors vectors containing containing either either an an N- N-terminalterminal signal signal sequence sequence (SigTAD1) (SigTAD1) or ora fulla full length length sequence sequence of ofTAD1 TAD1 fused fused with with synthetic synthetic green green fluorescent fluorescent protein protein (GFP) (GFP) (35S::SigTAD1(35S::SigTAD1-GFP-GFP or or 35S::TAD1 35S::TAD1-GFP)-GFP) were were introduced introduced to toand and transiently transiently expressed expressed in onionin onion epid epidermalermal cells. cells.Localization Localization of the proteins of the proteins was observed was observed with fluorescent with fluorescent micros- copy.microscopy. When the When onion the cells onion were cells bombarded were bombarded with the with 35S::GFP the 35S::GFP vector as vector a control, as a control,green fluorescencegreen fluorescence was observed was observed in the cytoplasm in the cytoplasm and nucleus and nucleus (Figure (Figure 2A). Onion2A). Onion cells cellsthat werethat b wereombarded bombarded with either with either35S::TAD1 35S::TAD1-GFP-GFP or 35S::SigTAD1 or 35S::SigTAD1-GFP-GFP displayed displayed GFP fluo- GFP rescencefluorescence,, which which localized localized in the inouter the outerlayer of layer the ofcell the (Figure cell (Figure 2B,C).2 B,C).Since Sincethere therewas little was differencelittle difference between between TAD1 TAD1-GFP-GFP and andSigTAD1 SigTAD1-GFP,-GFP, it was it was concluded concluded
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